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Pediatric Hematology and Oncology, 30:239–245, 2013 Copyright C Informa Healthcare USA, Inc. ISSN: 0888-0018 print / 1521-0669 online DOI: 10.3109/08880018.2012.763077 HEMATOLOGY IN INFANTS Iron Deficiency Anemia in Infants: Does It Really Affect the Myocardial Functions? Bulent Alioglu, 1 Ibrahim Ilker Cetin, 2 Zeynep Sengul Emeksiz, 3 Nermin Dindar, 4 Esra Tapci, 3 and Yildiz Dallar 3 1 Department of Pediatric Hematology, Directors of Regional Blood Bank, Therapeutic Apheresis, and Hematology Laboratories, Ankara Training and Research Hospital, Ankara, Turkey; 2 The Clinic of Pediatric Cardiology, Ankara Child Health, Hematology, Oncology, Education and Research Hospital, Ankara, Turkey; 3 Department of Pediatrics, Ankara Training and Research Hospital, Ankara, Turkey; 4 Department of Biochemistry, Ankara Training and Research Hospital, Ankara, Turkey The aim was to assess the myocardial functions in infants with iron deficiency anemia (IDA). The findings of 22 infants with IDA and 16 healthy infants were compared. Complete blood count in all infants, serum iron level, total iron binding capacity (TIBC), and serum ferritin level in patients were evaluated. Echocardiography with tissue Doppler imaging (TDI) was performed in all infants. The mean hemoglobin was 8.5 versus 11 g/dL, hematocrit was 26.7 versus 33.1% and the mean corpuscular volume (MCV) was 59.8 versus 72.2 fL in patients and controls, respectively. The me- dian serum iron level was 14.5 μg/dL, TIBC was 444 μg/dL, and serum ferritin level was 4.9 ng/mL in patients. There were significant differences between patients and controls for the myocardial performance indexes of the left ventricle (LV) (0.57 vs. 0.45, P < .05), interventricular septum (IVS) (0.56 vs. 0.48, P < .05), and the right ventricle (RV) (0.56 vs. 0.41, P < .05). The similar significances were also present for the ejection times (ET) of the LV (173.1 vs. 212.1 ms, P < .05), IVS (173.7 vs. 195.6 ms, P < .05), and RV (169.9 vs. 213.3 ms, P < .05). In spite of negatively significant correlations between hemoglobin, hematocrit, MCV and MPI, the correlations between these parameters and ET were positively significant. However, there were no correlations between serum iron level, TIBC, serum ferritin level, and the TDI parameters of patients. According to these findings, we could say that, the IDA affects the myocardial functions in a negative manner. Keywords iron deficiency anemia, myocardial performance, tissue Doppler imaging INTRODUCTION Iron deficiency anemia (IDA), is the most common anemia worldwide and most com- mon cause is the inadequate iron intake. IDA frequently affects children in preschool and school ages and preadolescents. Prevalence for preschool children aged between 5 and 8 years is 5.5%, whereas it is 2.6% for preadolescents [1]. IDA is a disease affecting many systems both hematologic and nonhematologic. It causes very serious complications such as anxiety, gastrointestinal symptoms, recur- rent infections, heart failure, tachycardia, dyspnea, diminished cellular immunity, loss Received 28 November 2012; accepted 28 December 2012; published online 2013. Address correspondence to Bulent Alioglu, MD, e Ministry of Health of Turkey, Ankara Training and Research Hospital, Ulucanlar Caddesi, Altindag, 06340 Ankara, Turkey. E-mail: [email protected] Pediatr Hematol Oncol Downloaded from informahealthcare.com by University of Waterloo on 11/06/14 For personal use only.

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Page 1: Iron Deficiency Anemia in Infants: Does It Really Affect the Myocardial Functions?

Pediatric Hematology and Oncology, 30:239–245, 2013Copyright C© Informa Healthcare USA, Inc.ISSN: 0888-0018 print / 1521-0669 onlineDOI: 10.3109/08880018.2012.763077

HEMATOLOGY IN INFANTS

Iron Deficiency Anemia in Infants: Does It ReallyAffect the Myocardial Functions?

Bulent Alioglu,1 Ibrahim Ilker Cetin,2 Zeynep Sengul Emeksiz,3

Nermin Dindar,4 Esra Tapci,3 and Yildiz Dallar3

1Department of Pediatric Hematology, Directors of Regional Blood Bank, TherapeuticApheresis, and Hematology Laboratories, Ankara Training and Research Hospital, Ankara,Turkey; 2The Clinic of Pediatric Cardiology, Ankara Child Health, Hematology, Oncology,Education and Research Hospital, Ankara, Turkey; 3Department of Pediatrics, AnkaraTraining and Research Hospital, Ankara, Turkey; 4Department of Biochemistry, AnkaraTraining and Research Hospital, Ankara, Turkey

The aim was to assess the myocardial functions in infants with iron deficiency anemia (IDA). Thefindings of 22 infants with IDA and 16 healthy infants were compared. Complete blood count inall infants, serum iron level, total iron binding capacity (TIBC), and serum ferritin level in patientswere evaluated. Echocardiography with tissue Doppler imaging (TDI) was performed in all infants.The mean hemoglobin was 8.5 versus 11 g/dL, hematocrit was 26.7 versus 33.1% and the meancorpuscular volume (MCV) was 59.8 versus 72.2 fL in patients and controls, respectively. The me-dian serum iron level was 14.5 μg/dL, TIBC was 444 μg/dL, and serum ferritin level was 4.9 ng/mLin patients. There were significant differences between patients and controls for the myocardialperformance indexes of the left ventricle (LV) (0.57 vs. 0.45, P < .05), interventricular septum (IVS)(0.56 vs. 0.48, P < .05), and the right ventricle (RV) (0.56 vs. 0.41, P < .05). The similar significanceswere also present for the ejection times (ET) of the LV (173.1 vs. 212.1 ms, P < .05), IVS (173.7 vs.195.6 ms, P < .05), and RV (169.9 vs. 213.3 ms, P < .05). In spite of negatively significant correlationsbetween hemoglobin, hematocrit, MCV and MPI, the correlations between these parameters andET were positively significant. However, there were no correlations between serum iron level, TIBC,serum ferritin level, and the TDI parameters of patients. According to these findings, we could saythat, the IDA affects the myocardial functions in a negative manner.

Keywords iron deficiency anemia, myocardial performance, tissue Doppler imaging

INTRODUCTION

Iron deficiency anemia (IDA), is the most common anemia worldwide and most com-mon cause is the inadequate iron intake. IDA frequently affects children in preschooland school ages and preadolescents. Prevalence for preschool children aged between5 and 8 years is 5.5%, whereas it is 2.6% for preadolescents [1].

IDA is a disease affecting many systems both hematologic and nonhematologic. Itcauses very serious complications such as anxiety, gastrointestinal symptoms, recur-rent infections, heart failure, tachycardia, dyspnea, diminished cellular immunity, loss

Received 28 November 2012; accepted 28 December 2012; published online 2013.Address correspondence to Bulent Alioglu, MD, The Ministry of Health of Turkey, Ankara Trainingand Research Hospital, Ulucanlar Caddesi, Altindag, 06340 Ankara, Turkey. E-mail:[email protected]

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of concentration, regression in mental scores, cognitive dysfunction, and decrease inschool success [2]. It is proved that some of these are temporary and some has lastingeffects.

In this study, the myocardial functions were evaluated in infants with IDA by usingechocardiography with tissue Doppler imaging (TDI).

PATIENTS AND METHODS

In the study, the data of 22 patients with isolated nutritional IDA with no other knowndisease and 16 healthy children free from anemia were analyzed prospectively. Themean age of patients was 1.4 ± 0.7 years and of healthy children was 1.4 ± 0.6 years. Inall patients, the hemoglobin (Hgb) value in complete blood count was < 9 gr/dL andserum iron, and ferritin levels are compatible with IDA. All these children were agedbetween 6 months and 2 years, and submitted to Ministry of Health Ankara Trainingand Research Hospital Pediatric Outpatient Clinics and Pediatric Haematology De-partment between December 2009 and April 2010.

Chronological ages, anthropometric features (body length and weight), body massindexes, standard deviation scores for length and weight, accompanying diseases, pre-maturity, low birth weight, chronic diseases, drug usage, perinatal bleeding, diarrhea,constipation, early solid food feeding, anxiety, iron treatment, allergic story, and his-tory for the usage of drugs decreasing iron absorption were recorded for all.

The inclusion criteria were being a term infant with a diagnosis of IDA. Ex-clusion criteria were uncontrollable diseases, infection, anemia of chronic disease,thalassemia, cardiac diseases, other hematologic diseases, renal diseases, hypothy-roidism, gastrointestinal system diseases, usage of drugs disturbing iron absorption,prior regular iron treatment and failure to get iron treatment regularly, and anti-inflammatory treatment.

Peripheral blood samples were taken to evaluate complete blood count in all in-fants and serum iron level, total iron binding capacity (TIBC) and serum ferritin levelin patients. The complete blood count of all participating patients was done using dailycalibrated hemocytometer (LH-780, Beckman Coulter, USA). Hgb, hematocrit (Hct),white blood cell count, platelet count, mean erythrocyte volume, mean erythrocyteHgb, mean corpuscular Hgb concentration, red blood cell distribution width, and ab-solute reticulocyte count was measured from venous blood sample taken into stan-dard tubes containing 0.072 mL 7.5% K3 ethylene diaminetetraacetic acid solution.For iron, TIBC, iron saturation, and ferritin analysis, we took 1 cc blood sample intobiochemical analysis tube.

Echocardiography together with TDI was performed in all infants. Echocardio-graphic studies were performed on “Vivid I” (GE) ultrasound system, using 7 MHztransducers. Tissue Doppler measurements were performed according to previouslydefined parameters, on basal segments [3,4]. The myocardial velocities during systole,early diastole and late diastole were recorded. The isovolumic contraction time is de-fined as the time period between the end of the Am wave and the beginning of the Smwave. The isovolumic relaxation time is defined as the time period between the end ofthe Sm wave and the beginning of the Em wave. Ejection time (ET) is measured as theduration of ventricular outflow. The MPI is defined as the sum of isovolumic contrac-tion and relaxation times, divided by ET. The mean values were recorded by averagingthe results of three consecutive measurements.

This study is approved by The Education Planning and Coordination Board of ourhospital (Decision No: 2748) at 02.12.2009.

Statistical analysis was performed by using the “SPSS for Windows” software. Datawere analyzed for comparison between two groups by using “Mann–Whitney U test”

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Iron Deficiency Anemia and Myocardial Functions

TABLE 1 Hematologic and Iron Parameters of Patients and Controls

Patients (n = 22) Controls (n = 16) P

Hgb (g/dL) 8.5 ± 0.5 (7.8–9.5) 11 ± 0.6 (10.1–12.1) <.05Hct (%) 26.7 ± 1.7 (24–29.5) 33.1 ± 1.8 (30.4–36.4) <.05MCV (fL) 59.8 ± 5.5 (50–72.8) 72.2 ± 2.4 (68.4–77.1) <.05Serum iron (μg/dL) 20.7 ± 20.1 (4–97) (14.5)∗ –TIBC (μg/dL) 432.2 ± 59.3 (304–547) (444) –Serum ferritin (ng/mL) 20.9 ± 38.9 (0.6–135) (4.9) –

∗Mean ± SD (min-max) (median).

and for correlation analysis “Pearson and Spearman correlation tests” were used. Sta-tistical significance was defined as P < .05.

RESULTS

The hematologic parameters of patients and controls are presented in Table 1. Themean Hgb was 8.5 versus 11 g/dL, Hct was 26.7 versus 33.1% and the mean corpus-cular volume (MCV) was 59.8 versus 72.2 fL in patients and controls, respectively. Themedian serum iron level was 14.5 μg/dL, TIBC was 444 μg/dL, and serum ferritin levelwas 4.9 ng/mL in patients.

The TDI findings of patients and controls are presented in Tables 2–4. There weresignificant differences between patients and controls for the myocardial performanceindexes (MPI) of the left ventricle (LV) (0.57 vs. 0.45, P < .05), interventricular septum(IVS) (0.56 vs. 0.48, P < .05), and the right ventricle (RV) (0.56 vs. 0.41, P < .05). The sim-ilar significances were also present for the ET of the LV (173.1 vs. 212.1 ms, P < .05), IVS(173.7 vs. 195.6 ms, P <.05), and RV (169.9 vs. 213.3 ms, P < .05). The MPI distributionsin patients and controls for LV, IVS, and RV are presented in Figures 1–3, respectively.In spite of negatively significant correlations between Hgb, Hct, MCV, and MPI, thecorrelations between these parameters and ET were positively significant (Table 5).However, there were no correlations between serum iron level, TIBC, serum ferritinlevel, and the TDI parameters of patients.

DISCUSSION

IDA has various hematological and nonhematological complications. Negative effectson cardiovascular system are one of the most important nonhematological compli-cations. It causes important cardiac complications such as diminished work capacity,

TABLE 2 Left Ventricular TDI Findings of Patients and Controls

Patients (n = 22) Controls (n = 16) P

LV Sm (cm/s) 7.7 ± 1.3 (6–10)∗ 7.7 ± 1.1 (6–10) >.05LV Em (cm/s) 14.3 ± 2.5 (7–18) 11.8 ± 1.7 (9–15) <.05LV Am (cm/s) 7.7 ± 1.8 (5–11) 8.1 ± 1.2 (6–10) >.05LV IRT (ms) 48.6 ± 8.7 (35–67) 46.3 ± 4 (38–52) >.05LV ICT (ms) 50.1 ± 13.1 (36–96 ± 4.3 (41–59) >.05LV ET (ms) 173.1 ± 27.4 (130–216) 212.1 ± 19.4 (169–243) <.05LV MPI 0.57 ± 0.1 (0.4–0.8) 0.45 ± 0.06 (0.4–0.6) <.05

Abbreviations: Sm, myocardial rate during systole; Em, myocardial rate during early diastole; Am,myocardial rate during late diastole; ICT, isovolumic contraction time; IRT, isovolumic relaxationtime.

∗Mean ± SD (min-max).

Copyright C© Informa Healthcare USA, Inc.

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FIGURE 1 LV MPI distribution in patients and controls.

reduced cardiac output, increase in heart rate, changes in electrocardiography, car-diac dilation or hypertrophy, and heart failure [1–4]. These complications are signifi-cant in deep anemia period. This situation is related with diminished oxygen transportcapacity into tissue and compensatory hemodynamic mechanisms.

Cardiac complications caused by anemia are not related with only IDA. Car-diac complications caused by anemia are especially well defined in patients with

FIGURE 2 IVS MPI distribution in patients and controls.

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Iron Deficiency Anemia and Myocardial Functions

FIGURE 3 RV MPI distribution in patients and controls.

thalassemia major and sickle cell anemia [5–8]. But cardiac complications causedby thalassemia major are related to cardiac iron deposition besides compensatoryhemodynamic mechanisms [9,10]. In patients with sickle cell anemia cardiac compli-cations such as increase in left atrium diameter and LV preejection period, dilatationin left atrium and LV cavities, and increase in LV mass and LV dysfunction are defined[11]. Besides these in patients with sickle cell anemia ischemic changes in electrocar-diography, diminished LV end-diastolic volume and abnormality in wall movementsare determined.

In our study, it was aimed to compare effects of severe IDA seen in breast feed-ing child period on ventricular functions by using MPI. So TDI was performed. It isreported that TDI is complementary in showing myocardial functions and in someaspects, it has superior features [12–14]. Especially not effecting from preload andpossibility of segmental analysis of myocardial functions are the most importantsuperiorities.

TABLE 3 IVS TDI Findings of Patients and Controls

Patients Controls P

IVS Sm (cm/s) 6.8 ± 1.1 (5–9)∗ 6.9 ± 0.9 (5–8) >.05IVS Em (cm/s) 11.8 ± 1.6 (9–15) 11.3 ± 1.9 (9–15) >.05IVS Am (cm/s) 7.4 ± 2.1 (4–13) 7.1 ± 1.3 (5–10) >.05IVS IRT (ms) 46.9 ± 8.7 (33–67) 44.9 ± 4 (41–54) >.05IVS ICT (ms) 47.9 ± 10.2 (37–74) 48.4 ± 7 (37–62) >.05IVS ET (ms) 173.7 ± 31.4 (115–238) 195.6 ± 27.5 (148–233) <.05IVS MPI 0.56 ± 0.12 (0.32–0.76) 0.48 ± 0.1 (0.38–0.57) <.05

Abbreviations: Sm, myocardial rate during systole; Em, myocardial rate during early diastole; Am,myocardial rate during late diastole; ICT, isovolumic contraction time; IRT, isovolumic relaxationtime.

∗Mean ± SD (min-max).

Copyright C© Informa Healthcare USA, Inc.

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TABLE 4 Right Ventricular TDI Findings of Patients and Controls

Patients Controls P

RV Sm (cm/s) 8.9 ± 2 (5–12)∗ 9 ± 1.1 (7–11) >.05RV Em (cm/s) 13.7 ± 3.2 (9–19) 13.5 ± 2.1 (10–17) >.05RV Am (cm/s) 8.8 ± 3 (5–15) 8.9 ± 1.2 (7–11) >.05RV IRT (ms) 45.9 ± 5.3 (36–55) 42.3 ± 4 (37–52) >.05RV ICT (ms) 48.7 ± 8.6 (38–70) 45 ± 4 (37–52) >.05RV ET (ms) 169.9 ± 27.6 (130–212) 213.3 ± 15.5 (177–232) <.05RV MPI 0.56 ± 0.07 (0.45–0.75) 0.41 ± 0.04 (0.35–0.5) <.05

Abbreviations: Sm, myocardial rate during systole; Em, myocardial rate during early diastole; Am,myocardial rate during late diastole; ICT, isovolumic contraction time; IRT, isovolumic relaxationtime.

∗Mean ± SD (min-max).

TABLE 5 The Correlations Between the Hematologic and TDI Parameters of All Infants

LV MPI LV ET IVS MPI IVS ET RV MPI RV ET

Hgb −0.6∗ 0.6 −0.5 0.5 −0.8 0.7< 0.0001∗ < 0.0001 < 0.005 < 0.001 < 0.0001 < 0.0001

Hct −0.6 0.6 −0.5 0.5 −0.8 0.7< 0.0001 < 0.0001 < 0.001 < 0.001 < 0.0001 < 0.0001

MCV −0.6 0.6 −0.4 0.4 −0.7 0.6< 0.0001 < 0.001 < 0.01 < 0.01 < 0.0001 < 0.001

∗r and P values.

In our study, MPIs of LV, RV, and IVS are significantly higher in patients with IDAthan in healthy control group. Besides this, ETs of LV, RV, and IVS are significantly lowerin patients than in healthy control group. In patients with IDA, especially significantdecrease in LV volume index and cardiac index, increase in LV end diastolic pressureand left atrium diameter, and extension in LV diastolic filling parameters have beenreported [15,16]. Authors suggest that LV dysfunction and circulatory congestion seenin these patients are related to these above mentioned factors. Our study is importantbecause of being the first study in literature that shows decrease in myocardial func-tions by using MPI in breast feeding children with IDA.

So, ventricular functions are affected negatively in patients with IDA. MyocardialET and performance index could be used to assess the myocardial functions in thesepatients.

Declaration of Interest

The authors report no conflicts of interest. The authors alone are responsible for thecontent and writing of the paper.

REFERENCES

[1] Lanzkowsky P. Iron-deficiency anemia. Lanzkowsky Manuel of Pediatric Hematology and Oncology.3rd ed. New York: Churchill Livingstone; 2000:33–49.

[2] Glader B. Anemias of inadequate production. In: Kliegman RM, Behrman RE, Jenson HB, StantonBF, eds. Nelson Textbook of Pediatrics. 18th ed. Philadelphia: WB Saunders; 2007:2006–2018. 15.). Itis proved that some of these are temporary and some has lasting effects.

[3] Karahan Z, Iltumur K, Toprak N. Kalp yetersizligi ve anemi. Turk Kardiyoloji Dernegi Arsivi.2006;34:59–65.

[4] Cook JD, Skikne BS. Iron deficiency: definition and diagnosis. J Intern Med. 2000;226:349–355.

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Iron Deficiency Anemia and Myocardial Functions

[5] Kremastinos DT, Tsiapras DP, Kostopoulou AG, et al. NT-proBNP levels and diastolic dysfunction inβ thalassemia major patients. Eur J Heart Fail. 2007;9:531–536.

[6] Silvilairat S, Sittiwangkul R, Pongprot Y, et al. Tissue Doppler echocardiography reliably reflectsseverity of iron overload in pediatric patients with β thalassemia. Eur J Echocardiogr. 2008;9:368–372.

[7] Caldas MC, Meira ZA, Barbosa MM. Evaluation of 107 patients with sickle cell anemia through tissueDoppler and myocardial performance index. J Am Soc Echocardiogr. 2008;21:1163–1167.

[8] Hankins JS, McCarville MB, Hillenbrand CM, et al. Ventricular diastolic dysfunction in sickle cellanemia is common but not associated with myocardial iron deposition. Pediatr Blood Cancer.2010;55:495–500.

[9] Hamdy AM. Use of strain and tissue velocity imaging for early detection of regional myocardial dys-function in patients with beta thalassemia. Eur J Echocardiogr. 2007;8:102–109.

[10] Ucar T, Ileri T, Atalay S, et al. Early detection of myocardial dysfunction in children with beta-thalassaemia major. Int J Cardiovasc Imaging. 2009;25:379–386.

[11] Zilberman MV, Du W, Das S, Sarnaik SA. Evaluation of left ventricular diastolic function in pediatricsickle cell disease patients. Am J Hematol. 2007;82:433–438.

[12] Mishiro Y, Oki T, Yamada H, et al. Use of angiotensin II stress pulsed tissue Doppler imaging to eval-uate regional left ventricular contractility in patients with hypertrophic cardiomyopathy. J Am SocEchocardiogr. 2000;13:1065–1073.

[13] Garcia-Fernandez MA, Zamorano J, Azevedo J (eds). Doppler Tissue Imaging. Madrid: McGraw-Hill;1998.

[14] Sengupta PP, Mohan JC, Pandian NG. Tissue doppler echocardiography: principles and applications.Indian Heart J. 2002;54;368–378.

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